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Mitochondrial Genome Diversity in the Central Siberian Plateau with Particular bioRxiv preprint doi: https://doi.org/10.1101/656181; this version posted May 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Mitochondrial Genome Diversity in the Central Siberian Plateau with Particular Reference to Prehistory of Northernmost Eurasia S. V. Dryomov*,1, A. M. Nazhmidenova*,1, E. B. Starikovskaya*,1, S. A. Shalaurova1, N. Rohland2, S. Mallick2,3,4, R. Bernardos2, A. P. Derevianko5, D. Reich2,3,4, R. I. Sukernik1. 1 Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, SBRAS, Novosibirsk, Russian Federation 2 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA 3 Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA 4 Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA 5 Institute of Archaeology and Ethnography, SBRAS, Novosibirsk, Russian Federation Corresponding author: Rem Sukernik ([email protected]) * These authors contributed equally to this work. bioRxiv preprint doi: https://doi.org/10.1101/656181; this version posted May 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Abstract The Central Siberian Plateau was last geographic area in Eurasia to become habitable by modern humans after the Last Glacial Maximum (LGM). Through comprehensive mitochondrial DNA genomes retained in indigenous Siberian populations, the Ket, Tofalar, and Todzhi - we explored genetic links between the Yenisei-Sayan region and Northeast Eurasia over the last 10,000 years. Accordingly, we generated 218 new complete mtDNA sequences and placed them into compound phylogenies along with 7 newly obtained and 70 published ancient mt genomes. Our findings reflect the origins and expansion history of mtDNA lineages that evolved in South-Central Siberia, as well as multiple phases of connections between this region and distant parts of Eurasia. Our result illustrates the importance of jointly sampling modern and prehistoric specimens to fully measure the past genetic diversity and to reconstruct the process of peopling of the high latitudes of the Siberian subcontinent. Although modern humans began colonizing sub-arctic and arctic Siberia 45,000 years ago, most archaeological sites postdate 12 kya, with the exception of episodic incursions to the north of Eurasia during the warm phases, with the settlements primary limited to cryptic refugia both in eastern Europe and Asia (reviewed by Pitulko et al., 2017 [1]). During the last millennium, the Central Siberian Plateau, bounded by the Yenisei River to the west, the North Siberian Lowland to the north, the Verkhoynsk Mountains to the east, and the Sayan Mountains and Lake Baikal to the south, has been shaped by key episodes that have had major impacts on human migrations, admixture, and population replacement. At the end of the 15th century, when Russians first crossed the Ural Mountains in substantial numbers, dozens of indigenous tribes and bands with 2 bioRxiv preprint doi: https://doi.org/10.1101/656181; this version posted May 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. markedly different ways of life and subsistence were widespread throughout Siberia [2,3]. Soon after, some of these groups became extinct or underwent marked postcontact decimation and admixture while others only diminished in number, their territories shrinking to small patches of their former distributions. Two strata are recognized in the aboriginal Siberian population: an ancient layer and a comparatively new one, or the “Old Siberians” versus “Neosiberians” [4,5]. Most of the “Old Siberians” who spoke languages belonging to linguistic outliers, such as Omok (an extinct Yukaghir language spoken as late as the 18th century in the lower Kolyma and Indigirka valleys), have been greatly reduced in number, and their cultures have been brought under the domination of the more populous Neosiberians: Tungusic, Turkic or Mongolian tribes, all relative newcomers to the region [2,3,5,6]. Nonetheless, groups of Old Siberians still persist in remote “pockets” of Siberia in the form of anthropological isolates, usually representing the now-amalgamating remnants of small, previously distinct tribes and lineages. The study of mitochondrial DNA variation to ascertain their origin and affinities, as well as their relationship to the first Americans, has been a subject of intensive study since the early 1990s [7-9]. Candidate founding lineages for Native American mtDNA haplogroups were identified by identifying similar haplogroups in Eurasia [10-14]. For instance, unique mtDNA sequences (haplogroups B4b1a, D4h2, and C1a) linked to Native American B2, D4h3a, and C1, respectively, were attested using complete mtDNA sequences [10-12,14]. A complete catalogue of mtDNA variation in the “Old-Siberians” is therefore important not just for understanding the specific history of Siberia, but also the ancestry of peoples of the New World. A central concern of this study is disentangling ancestries from different sources that mixed at different time points in the past to provide a better understanding of the 3 bioRxiv preprint doi: https://doi.org/10.1101/656181; this version posted May 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. genetic interactions between and within Siberian populations. Accordingly, we focused on mitochondrial DNA genome diversity in the Yenisei-Sayan autochthonous populations, primarily the Ket, Tofalar, and Todzhi (Fig. 1). Ket are now the sole surviving member of the Yeniseian language family, speaking a unique language that does not easily fit into any known phyla and is unrelated to any other Siberian language [15]. Their related tribes, the Assan, Arin, and Kott, disappeared about 200 years after their first contact with Russians. In this region, the Ket is the last tribe to retain their original language and until recent times subsisted entirely on hunting, fishing, and the gathering of wild plants [2,16,17]. The Tofalar and Todzhi languages whose members originally spoke Samoyed belong to the subgroup of Turkic languages confined to the upper Yenisei area [18-20], where they may have had ample opportunity to exchange genes with the Ket or related tribes (Lopatin, 1940 [5], and references therein). We compared mitochondrial DNA present-day diversity from these groups with complete mitochondrial genomes from ancient samples from the region and placed them into combined genealogical trees. We used these updated genealogies to trace ancestral relationships between populations sharing subhaplogroup-specific mutations. We used the results to reconstruct expansions (preponderantly from south to north) as well as contractions of populations, thus shedding new light on northeastern Eurasia's past. Populations and samples Ket - Formerly called Yenisei Ostyak (the census of 1897 recorded 988 persons), the Ket people are thought to be descendants of some of the earliest inhabitants of Central Siberia, while all of their present-day neighbors seem to be relative newcomers. In the 18th century part of the Ket were forcibly moved to the lands between the Ob and Yenisei Rivers, where the Selkup belonging to the Samoyed group 4 bioRxiv preprint doi: https://doi.org/10.1101/656181; this version posted May 31, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. of the Uralic language family lived [2,5,16]. Until recently, there were ~500 Ket living in a few riverside villages in the middle reaches of the Yenisey; as in the past, many survive as seasonal hunters, trappers, and fishermen. The remnants of the Southern (Upper) Ket, whose ancestors are believed to have originated from the Podkamennaya Tunguska region, have been almost completely integrated into the expanding Evenki [17]. We integrated our newly obtained mtDNA sequences from previously collected DNA samples with previously published data [21] and collected new DNA samples from indivduals residing in August of 2014 in the villages of Turukhansk and Kellog (Turukhansk District, Krasnoyarsk Region, Russian Federation). The total Ket sample subjected to complete mtDNA sequencing was 38 individuals. Based on self-reported ancestry, verified by senior members of related families, we determined that the overwhelming majority of the Ket have been extensively admixed with Russians. A substantial proportion of the Ket were not completely certain of their maternal ancestry in terms of Ket, Selkup, or Evenki origin. Tofalar – Fewer than 400 Tofalar, who are reindeer breeders and hunters, inhabit the northern slopes of the eastern Sayan Mountains, along the rivers Uda, Gutara, and Nerkha. They originally
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